Skip to main content
Log in

Effects of Time on Phenolics and in vitro Bioactivity in Autoclave Extraction of Graviola (Annona muricata) Leaf

  • Research Paper
  • Biomedical Engineering
  • Published:
Biotechnology and Bioprocess Engineering Aims and scope Submit manuscript

Abstract

We investigated the effects of different autoclave extraction times (1-6 h) on the antioxidant, antidiabetic, and anti-inflammatory activities of phenolic compounds isolated from graviola (Annona muricata) leaves. In terms of yield and content of total polyphenols, total flavonoids, rutin, and kaempferol-3-O-rutinoside, the optimal extraction time was 4 h. At this time point, water extracts from graviola leaves (WEG) exhibited the highest DPPH radical scavenging activity, ferric reducing antioxidant power, and α-glucosidase inhibitory activity. The α-glucosidase inhibitory activity of WEG was significantly stronger than that of acarbose. Furthermore, WEG significantly suppressed lipopolysaccharide-induced nitric oxide production in RAW 264.7 cells and inhibited UVB-induced activator protein-1 (AP-1)-dependent transcription in human keratinocytes. In conclusion, WEG can be used as functional food ingredients in the food industry.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Leboeuf, M., A. Caré, M. E. Tohami, J. Pusset, P. Forgacs, and J. Provost (1982) Alkaloids of annonaceae. XXXV. alkaloids of Desmos tiebaghiensis. J. Nat. Prod. 45: 617–623.

    Article  CAS  Google Scholar 

  2. Ayaz, F. A., S. Hayirlioglu-Ayaz, J. Gruz, O. Novak, and M. Strnad (2005) Separation, characterization, and quantitation of phenolic acids in a little-known blueberry (Vaccinium arctostaphylos L.) fruit by HPLC-MS. J. Agric. Food Chem. 53: 8116–8122.

    Article  CAS  Google Scholar 

  3. Nessa, F., Z. Ismail, S. Karupiah, and N. Mohamed (2005) RP-HPLC method for the quantitative analysis of naturally occurring flavonoids in leaves of Blumea balsamifera DC. J. Chromatogr. Sci. 43: 416–420.

    Article  CAS  Google Scholar 

  4. Lee, C. H., C. G. Krueger, J. D. Reed, and M. P. Richards (2006) Inhibition of hemoglobin-mediated lipid oxidation in washed fish muscle by cranberry components. Food Chem. 99: 591–599.

    Article  CAS  Google Scholar 

  5. Bansal, P., P. Paul, J. Mudgal, P. G. Nayak, S. T. Pannakal, K. I. Priyadarsini, and M. K. Unnikrishnan (2012) Antidiabetic, antihyperlipidemic and antioxidant effects of the flavonoid rich fraction of Pilea microphylla (L.) in high fat diet/streptozotocin-induced diabetes in mice. Exp. Toxicol. Pathol. 64: 651–658.

    Article  CAS  Google Scholar 

  6. Nawwar, M., N. Ayoub, S. Hussein, A. Hashim, R. El-Sharawy, K. Wende, M. Harms, and U. Lindequist (2012) A flavonol triglycoside and investigation of the antioxidant and cell stimulating activities of Annona muricata Linn. Arch. Pharm. Res. 35: 761–767.

    Article  CAS  Google Scholar 

  7. Son, Y. R., E. H. Choi, G. T. Kim, T. S. Park, and S. M. Shim (2016) Bioefficacy of Graviola leaf extracts in scavenging free radicals and upregulating antioxidant genes. Food Funct. 7: 861–871.

    Article  CAS  Google Scholar 

  8. Acésio, N. O., G. S. Carrijo, T. H. Batista, J. L. Damasceno, M. B. Côrrea, M. G. Tozatti, W. R. Cunha, and D. C. Tavares (2017) Assessment of the antioxidant, cytotoxic, and genotoxic potential of the Annona muricata leaves and their influence on genomic stability. J. Toxicol. Environ. Health A. 80: 1290–1300.

    Article  Google Scholar 

  9. Naczk, M. and F. Shahidi (2004) Extraction and analysis of phenolics in food. J. Chromatrogr. A. 1054: 95–111.

    Article  CAS  Google Scholar 

  10. Arya, V., N. Thakur, and C. P. Kashyap (2012) Preliminary phytochemical analysis of the extracts of Psidium leaves. J. Pharmacogn. Phytochem. 1: 1–5.

    Google Scholar 

  11. Budaraju, S., K. Mallikarjunan, G. Annor, T. Schoenfuss, and R. Raun (2018) Effect of pre-treatments on the antioxidant potential of phenolic extracts from barley malt rootlets. Food Chem. 266: 31–37.

    Article  CAS  Google Scholar 

  12. Mittal, M., M. R. Siddiqui, K. Tran, S. P. Reddy, and A. B. Malik (2014) Reactive oxygen species in inflammation and tissue injury. Antioxid. Redox Signal. 20: 1126–1167.

    Article  CAS  Google Scholar 

  13. Lee, J., S. J. Ha, H. J. Lee, M. J. Kim, J. H. Kim, Y. T. Kim, K. M. Song, Y. J. Kim, H. K. Kim, and S. K. Jung (2016) Protective effect of Tremella fuciformis Berk extract on LPS-induced acute inflammation via inhibition of the NF-κB and MAPK pathways. Food Funct. 7: 3263–3272.

    Article  CAS  Google Scholar 

  14. Ha, S. J., J. Lee, J. Park, Y. H. Kim, N. H. Lee, Y. E. Kim, K. M. Song, P. S. Chang, C. H. Jeong, and S. K. Jung (2018) Syringic acid prevents skin carcinogenesis via regulation of NoX and EGFR signaling. Biochem. Pharmacol. 154: 435–445.

    Article  CAS  Google Scholar 

  15. Jung, S. K., K. W. Lee, S. Byun, N. J. Kang, S. H. Lim, Y. S. Heo, A. M. Bode, G. T. Bowden, H. J. Lee, and Z. Dong (2008) Myricetin suppresses UVB-induced skin cancer by targeting Fyn. Cancer Res. 68: 6021–6029.

    Article  CAS  Google Scholar 

  16. Laksmitawati, D. R., A. P. Prasanti, N. Larasinta, G. A. Syauta, R. Hilda, H. U. Ramadaniati, A. Widyastuti, N. Karami, M. Arni, D. D. Rihibiha, H. S. W. Kusuma, and W. Widowati (2016) Anti-inflammatory potential of gandarusa (Gendarussa vulgaris Nees) and soursoup (Annona muricata L) extracts in LPS stimulated-macrophage cell (RAW264. 7). J. Nat. Rem. 16: 73–81.

    Google Scholar 

  17. Moghadamtousi, S. Z., E. Rouhollahi, M. Hajrezaie, H. Karimian, M. A. Abdulla, and H. A. Kadir (2015) Annona muricata leaves accelerate wound healing in rats via involvement of Hsp70 and antioxidant defence. Int. J. Surg. 18: 110–117.

    Article  Google Scholar 

  18. AACC (1995) Approved Method of the AACC. 10th ed. St. American Association of Cereal Chemists, St. Paul, MN, USA.

    Google Scholar 

  19. Kähkönen, M. P., A. I. Hopia, H. J. Vuorela, J. P. Rauha, K. Pihlaja, T. S. Kujala, and M. Heinonen (1999) Antioxidant activity of plant extracts containing phenolic compounds. J. Agric. Food Chem. 47: 3954–3962.

    Article  Google Scholar 

  20. Quettier-Deleu, C., B. Gressier, J. Vasseur, T. Dine, C. Brunet, M. Luyckx, M. Cazin, J. C. Cazin, F. Bailleul, and F. Trotin (2000) Phenolic compounds and antioxidant activities of buckwheat (Fagopyrum esculentum Moench) hulls and flour. J. Ethnopharmacol. 72: 35–42.

    Article  CAS  Google Scholar 

  21. Liu, P., H. Kallio, and B. Yang (2014) Flavonol glycosides and other phenolic compounds in buds and leaves of different varieties of black currant (Ribes nigrum L.) and changes during growing season. Food Chem. 160: 180–189.

    Article  CAS  Google Scholar 

  22. Ferruzzi, M. G., V. Böhm, P. D. Courtney, and S. J. Schwartz (2002) Antioxidant and antimutagenic activity of dietary chlorophyll derivatives determined by radical scavenging and bacterial reverse mutagenesis assays. J. Food Sci. 67: 2589–2595.

    Article  CAS  Google Scholar 

  23. Benzie, I. F. and J. J. Strain (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal. Biochem. 239: 70–76.

    Article  CAS  Google Scholar 

  24. Zhang, L., S. Hogan, J. Li, S. Sun, C. Canning, S. J. Zheng, and K. Zhou (2011) Grape skin extract inhibits mammalian intestinal α-glucosidase activity and suppresses postprandial glycemic response in streptozocin-treated mice. Food Chem. 126: 466–471.

    Article  CAS  Google Scholar 

  25. Vergara-Salinas, J. R., J. Pérez-Jiménez, J. L. Torres, E. Agosin, and J. R. Pérez-Correa (2012) Effects of temperature and time on polyphenolic content and antioxidant activity in the pressurized hot water extraction of deodorized thyme (Thymus vulgaris). J. Agric. Food Chem. 60: 10920–10929.

    Article  CAS  Google Scholar 

  26. Palma, M., Z. Piñeiro, and C. G. Barroso (2001) Stability of phenolic compounds during extraction with superheated solvents. J. Chromatogr. A. 921: 169–174.

    Article  CAS  Google Scholar 

  27. Biesaga, M. (2011) Influence of extraction methods on stability of flavonoids. J. Chromatogr. A. 1218: 2505–2512.

    Article  CAS  Google Scholar 

  28. Gavamukulya, Y., F. Abou-Elella, F. Wamunyokoli, and H. AEl-Shemy (2014) Phytochemical screening, anti-oxidant activity and in vitro anticancer potential of ethanolic and water leaves extracts of Annona muricata (Graviola). Asian Pac. J. Trop. Med. 7: S355–S363.

    Article  CAS  Google Scholar 

  29. Balkan, I. A., H. T. Doğan, G. Zengin, N. Colak, F. A. Ayaz, A. C. Gören, H. Kırmızıbekmez, and E. Yeşilada (2018) Enzyme inhibitory and antioxidant activities of Nerium oleander L. flower extracts and activity guided isolation of the active components. Ind. Crops. Prod. 112: 24–31.

    Article  Google Scholar 

  30. Jung, S. K., S. J. Ha, Y. A. Kim, J. Lee, T. G. Lim, Y. T. Kim, N. H. Lee, J. S. Park, M. H. Yeom, H. J. Lee, and K. W. Lee (2015) MLK 3 is a novel target of dehydroglyasperin D for the reduction in UVB-induced COX-2 expression in vitro and in vivo. J. Cell. Mol. Med. 19: 135–142.

    Article  CAS  Google Scholar 

  31. Jung, S. K., S. J. Ha, C. H. Jung, Y. T. Kim, H. K. Lee, M. O. Kim, M. H. Lee, M. Mottamal, A. M. Bode, K. W. Lee, and Z. Dong (2016) Naringenin targets ERK2 and suppresses UVB-induced photoaging. J. Cell. Mol. Med. 20: 909–919.

    Article  CAS  Google Scholar 

  32. Tadera, K., Y. Minami, K. Takamatsu, and T. Matsuoka (2006) Inhibition of α-glucosidase and α-amylase by flavonoids. J. Nutr. Sci. Vitaminol. 52: 149–153.

    Article  CAS  Google Scholar 

  33. Etxeberria, U., A. L. de la Garza, J. Campión, J. A. Martínez, and F. I. Milagro (2012) Antidiabetic effects of natural plant extracts via inhibition of carbohydrate hydrolysis enzymes with emphasis on pancreatic alpha amylase. Expert Opin. Ther. Targets. 16: 269–297.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Technology development Program (C0452780) funded by the Ministry of SMEs and Startups (MSS, Korea).

The authors declare no conflict of interest.

Neither ethical approval nor informed consent was required for this study.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Sung Keun Jung or Yoon Hyuk Chang.

Additional information

Publisher’s Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Choi, M., Kang, YR., Zu, H.D. et al. Effects of Time on Phenolics and in vitro Bioactivity in Autoclave Extraction of Graviola (Annona muricata) Leaf. Biotechnol Bioproc E 25, 9–15 (2020). https://doi.org/10.1007/s12257-019-0259-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12257-019-0259-3

Keywords

Navigation